Conformation of DNA GG intrastrand cross-link of antitumor oxaliplatin and its enantiomeric analog

. 2007 Dec 01 ; 93 (11) : 3950-62. [epub] 20070817

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid17704160
Odkazy

PubMed 17704160
PubMed Central PMC2084227
DOI 10.1529/biophysj.107.116996
PII: S0006-3495(07)71647-8
Knihovny.cz E-zdroje

Downstream processes that discriminate between DNA adducts of a third generation platinum antitumor drug oxaliplatin and conventional cisplatin are believed to be responsible for the differences in their biological effects. These different biological effects are explained by the ability of oxaliplatin to form DNA adducts more efficient in their biological effects. In this work conformation, recognition by HMG domain protein and DNA polymerization across the major 1,2-GG intrastrand cross-link formed by cisplatin and oxaliplatin in three sequence contexts were compared with the aid of biophysical and biochemical methods. The following major differences in the properties of the cross-links of oxaliplatin and cisplatin were found: i), the formation of the cross-link by oxaliplatin is more deleterious energetically in all three sequence contexts; ii), the cross-link of oxaliplatin bends DNA slightly but systematically less in all sequence contexts tested; iii), the affinity of HMG domain protein to the cross-link of oxaliplatin is considerably lower independent of the sequence context; and iv), the Klenow fragment of DNA polymerase I pauses considerably more at the cross-link of oxaliplatin in all sequence contexts tested. We have also demonstrated that the chirality at the carrier ligand of oxaliplatin can affect its biological effects.

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Lokich, J. 2001. What is the “best” platinum: cisplatin, carboplatin, or oxaliplatin? Cancer Invest. 19:756–760. PubMed

Boulikas, T., and M. Vougiouka. 2003. Cisplatin and platinum drugs at the molecular level. Oncol. Rep. 10:1663–1682 [review]. PubMed

Di Francesco, A. M., A. Ruggiero, and R. Riccardi. 2002. Cellular and molecular aspects of drugs of the future: oxaliplatin. Cell. Mol. Life Sci. 59:1914–1927. PubMed PMC

Johnson, N. P., J.-L. Butour, G. Villani, F. L. Wimmer, M. Defais, V. Pierson, and V. Brabec. 1989. Metal antitumor compounds: the mechanism of action of platinum complexes. Prog. Clin. Biochem. Med. 10:1–24.

Brabec, V., and J. Kasparkova. 2005. Modifications of DNA by platinum complexes: relation to resistance of tumors to platinum antitumor drugs. Drug Resist. Updat. 8:131–146. PubMed

Brabec, V. 2002. DNA modifications by antitumor platinum and ruthenium compounds: their recognition and repair. Prog. Nucleic Acid Res. Mol. Biol. 71:1–68. PubMed

Brabec, V., and J. Kasparkova. 2005. DNA interactions of platinum anticancer drugs. Recent advances and mechanisms of action. In Metal Compounds in Cancer Chemotherapy. J.-M. Perez-Martin, M. A. Fuertes, and C. Alonso, editors. Research Signpost, Trivandrum, Kerala, India. 187–218.

Vrana, O., V. Brabec, and V. Kleinwächter. 1986. Polarographic studies on the conformation of some platinum complexes: relations to anti-tumour activity. Anticancer Drug Des. 1:95–109. PubMed

Farrell, N., Y. Qu, and M. P. Hacker. 1990. Cytotoxicity and antitumor activity of bis(platinum) complexes: a novel class of platinum complexes active in cell lines resistant to both cisplatin and 1,2- diaminocyclohexane complexes. J. Med. Chem. 33:2179–2184. PubMed

Farrell, N. 1993. Nonclassical platinum antitumor agents: perspectives for design and development of new drugs complementary to cisplatin. Cancer Invest. 11:578–589. PubMed

Woynarowski, J. M., S. Faivre, M. C. S. Herzig, B. Arnett, W. G. Chapman, A. V. Trevino, E. Raymond, S. G. Chaney, A. Vaisman, M. Varchenko, and P. E. Juniewicz. 2000. Oxaliplatin-induced damage of cellular DNA. Mol. Pharmacol. 58:920–927. PubMed

Woynarowski, J. M., W. G. Chapman, C. Napier, M. C. S. Herzig, and P. Juniewicz. 1998. Sequence- and region-specificity of oxaliplatin adducts in naked and cellular DNA. Mol. Pharmacol. 54:770–777. PubMed

Reardon, J. T., A. Vaisman, S. G. Chaney, and A. Sancar. 1999. Efficient nucleotide excision repair of cisplatin, oxaliplatin, and bis-aceto-ammine-dichloro-cyclohexylamine-platinum(IV) (JM216) platinum intrastrand DNA diadducts. Cancer Res. 59:3968–3971. PubMed

Wu, H. I., J. A. Brown, M. J. Dorie, L. Lazzeroni, and J. M. Brown. 2004. Genome-wide identification of genes conferring resistance to the anticancer agents cisplatin, oxaliplatin, and mitomycin C. Cancer Res. 64:3940–3948. PubMed

Vaisman, A., M. Varchenko, A. Umar, T. A. Kunkel, J. I. Risinger, J. C. Barrett, T. C. Hamilton, and S. G. Chaney. 1998. The role of hMLH1, hMSH3, and hMSH6 defects in cisplatin and oxaliplatin resistance: correlation with replicative bypass of platinum-DNA adducts. Cancer Res. 58:3579–3585. PubMed

Vaisman, A., C. Masutani, F. Hanaoka, and S. G. Chaney. 2000. Efficient translesion replication past oxaliplatin and cisplatin GpG adducts by human DNA polymerase η. Biochemistry. 39:4575–4580. PubMed

Vaisman, A., and S. G. Chaney. 2000. The efficiency and fidelity of translesion synthesis past cisplatin and oxaliplatin GpG adducts by human DNA polymerase β. J. Biol. Chem. 275:13017–13025. PubMed

Bassett, E., A. Vaisman, J. M. Havener, C. Masutani, F. Hanaoka, and S. G. Chaney. 2003. Efficiency of extension of mismatched primer termini across from cisplatin and oxaliplatin adducts by human DNA polymerases beta and eta in vitro. Biochemistry. 42:14197–14206. PubMed

Spingler, B., D. A. Whittington, and S. J. Lippard. 2001. 2.4 Å crystal structure of an oxaliplatin 1,2-d(GpG) intrastrand cross-link in a DNA dodecamer duplex. Inorg. Chem. 40:5596–5602. PubMed

Wu, Y., P. Pradhan, J. Havener, G. Boysen, J. A. Swenberg, S. L. Campbell, and S. G. Chaney. 2004. NMR solution structure of an oxaliplatin 1,2-d(GG) intrastrand cross-link in a DNA dodecamer duplex. J. Mol. Biol. 341:1251–1269. PubMed

Wu, Y., D. Bhattacharyya, C. L. King, I. Baskerville-Abraham, S.-H. Huh, G. Boysen, J. A. Swenberg, B. Temple, S. L. Campbell, and S. G. Chaney. 2007. Solution structures of a DNA dodecamer duplex with and without a cisplatin 1,2-d(GG) intrastrand cross-link: comparison with the same DNA duplex containing an oxaliplatin 1,2-d(GG) intrastrand cross-link. Biochemistry. 46:6477–6487. PubMed PMC

Page, J. D., I. Husain, A. Sancar, and S. G. Chaney. 1990. Effect of the diaminocyclohexane carrier ligand on platinum adduct formation, repair, and lethality. Biochemistry. 29:1016–1024. PubMed

Fanizzi, F. P., F. P. Intini, L. Maresca, G. Natile, R. Quaranata, M. Coluccia, L. Di Bari, D. Giordano, and M. A. Mariggio. 1987. Biological activity of platinum complexes containing chiral centers on the nitrogen or carbon atoms of a chelate diamine ring. Inorg. Chim. Acta. 137:45–51.

Misset, J. L. 1998. Oxaliplatin in practice. Br. J. Cancer. 77(S4):4–7. PubMed PMC

Jamieson, E. R., and S. J. Lippard. 1999. Structure, recognition, and processing of cisplatin-DNA adducts. Chem. Rev. 99:2467–2498. PubMed

Benedetti, M., L. G. Marzilli, and G. Natile. 2005. Rotamer stability in cis-[Pt(diA)G2] complexes (diA=diamine derivative and G=guanine derivative) mediated by carrier-ligand amine stereochemistry as revealed by circular dichroism spectroscopy. Chem. Eur. J. 11:5302–5310. PubMed

Brabec, V., J. Reedijk, and M. Leng. 1992. Sequence-dependent distortions induced in DNA by monofunctional platinum(II) binding. Biochemistry. 31:12397–12402. PubMed

Stros, M. 1998. DNA bending by the chromosomal protein HMG1 and its high mobility group box domains. Effect of flanking sequences. J. Biol. Chem. 273:10355–10361. PubMed

Stros, M. 2001. Two mutations of basic residues within the N-terminus of HMG-1 B domain with different effects on DNA supercoiling and binding to bent DNA. Biochemistry. 40:4769–4779. PubMed

Kasparkova, J., K. J. Mellish, Y. Qu, V. Brabec, and N. Farrell. 1996. Site-specific d(GpG) intrastrand cross-links formed by dinuclear platinum complexes. Bending and NMR studies. Biochemistry. 35:16705–16713. PubMed

Brabec, V., M. Sip, and M. Leng. 1993. DNA conformational distortion produced by site-specific interstrand cross-link of trans-diamminedichloroplatinum(II). Biochemistry. 32:11676–11681. PubMed

Koo, H. S., H. M. Wu, and D. M. Crothers. 1986. DNA bending at adenine · thymine tracts. Nature. 320:501–506. PubMed

Bellon, S. F., and S. J. Lippard. 1990. Bending studies of DNA site-specifically modified by cisplatin, trans-diamminedichloroplatinum(II) and cis-Pt(NH3)2(N3-cytosine)Cl+. Biophys. Chem. 35:179–188. PubMed

Kasparkova, J., N. Farrell, and V. Brabec. 2000. Sequence specificity, conformation, and recognition by HMG1 protein of major DNA interstrand cross-links of antitumor dinuclear platinum complexes. J. Biol. Chem. 275:15789–15798. PubMed

Bailly, C., D. Gentle, F. Hamy, M. Purcell, and M. J. Waring. 1994. Localized chemical reactivity in DNA associated with the sequence-specific bisintercalation of echinomycin. Biochem. J. 300:165–173. PubMed PMC

Ross, S. A., and C. J. Burrows. 1996. Cytosine-specific chemical probing of DNA using bromide and monoperoxysulfate. Nucleic Acids Res. 24:5062–5063. PubMed PMC

Bailly, C., and M. J. Waring. 1997. Diethylpyrocarbonate and osmium tetroxide as probes for drug-induced changes in DNA conformation in vitro. In Drug-DNA Interaction Protocols. K. R. Fox, editor. Humana Press, Totowa, NJ. 51–79. PubMed

He, Q., U.-A. Ohndorf, and S. J. Lippard. 2000. Intercalating residues determine the mode of HMG1 domains A and B binding to cisplatin-modified DNA. Biochemistry. 39:14426–14435. PubMed

Lam, W. C., E. J. C. Van der Schans, L. C. Sowers, and D. P. Millar. 1999. Interaction of DNA polymerase I (Klenow fragment) with DNA substrates containing extrahelical bases: implications for proofreading of frameshift errors during DNA synthesis. Biochemistry. 38:2661–2668. PubMed

Patel, P. H., M. Suzuki, E. Adman, A. Shinkai, and L. A. Loeb. 2001. Prokaryotic DNA polymerase I: evolution, structure, and “base flipping” mechanism for nucleotide selection. J. Mol. Biol. 308:823–837. PubMed

Leharne, S. A., and B. Z. Chowdhry. 1998. Thermodynamic background to differential scanning calorimetry. In Biocalorimetry: Applications of Calorimetry in the Biological Sciences. J. E. Ladbury and B. Z. Chowdhry, editors. J. Wiley & Sons, Chichester, UK. 157–182.

Hofr, C., N. Farrell, and V. Brabec. 2001. Thermodynamic properties of duplex DNA containing a site-specific d(GpG) intrastrand crosslink formed by an antitumor dinuclear platinum complex. Nucleic Acids Res. 29:2034–2040. PubMed PMC

Hofr, C., and V. Brabec. 2001. Thermal and thermodynamic properties of duplex DNA containing site-specific interstrand cross-link of antitumor cisplatin or its clinically ineffective trans isomer. J. Biol. Chem. 276:9655–9661. PubMed

Pilch, D. S., S. U. Dunham, E. R. Jamieson, S. J. Lippard, and K. J. Breslauer. 2000. DNA sequence context modulates the impact of a cisplatin 1,2-d(GpG) intrastrand cross-link and the conformational and thermodynamic properties of duplex DNA. J. Mol. Biol. 296:803–812. PubMed

Brabec, V., K. Stehlikova, J. Malina, M. Vojtiskova, and J. Kasparkova. 2006. Thermodynamic properties of damaged DNA and its recognition by xeroderma pigmentosum group A protein and replication protein A. Arch. Biochem. Biophys. 446:1–10. PubMed

Poklar, N., D. S. Pilch, S. J. Lippard, E. A. Redding, S. U. Dunham, and K. J. Breslauer. 1996. Influence of cisplatin intrastrand crosslinking on the conformation, thermal stability, and energetics of a 20-mer DNA duplex. Proc. Natl. Acad. Sci. USA. 93:7606–7611. PubMed PMC

Malina, J., C. Hofr, L. Maresca, G. Natile, and V. Brabec. 2000. DNA interactions of antitumor cisplatin analogs containing enantiomeric amine ligands. Biophys. J. 78:2008–2021. PubMed PMC

Hofr, C., and V. Brabec. 2005. Thermal stability and energetics of 15-mer DNA duplex interstrand cross-linked by trans-diamminedichloroplatinum(II). Biopolymers. 77:222–229. PubMed

Ohndorf, U. M., M. A. Rould, Q. He, C. O. Pabo, and S. J. Lippard. 1999. Basis for recognition of cisplatin-modified DNA by high-mobility-group proteins. Nature. 399:708–712. PubMed

Zamble, D. B., and S. J. Lippard. 1999. The response of cellular proteins to cisplatin-damaged DNA. In Cisplatin. Chemistry and Biochemistry of a Leading Anticancer Drug. B. Lippert, editor. VHCA, Wiley-VCH, Zürich, Weinheim, Germany. 73–110.

Kasparkova, J., J. Zehnulova, N. Farrell, and V. Brabec. 2002. DNA interstrand cross-links of the novel antitumor trinuclear platinum complex BBR3464. Conformation, recognition by high mobility group domain proteins, and nucleotide excision repair. J. Biol. Chem. 277:48076–48086. PubMed

Kasparkova, J., O. Novakova, N. Farrell, and V. Brabec. 2003. DNA binding by antitumor trans-[PtCl2(NH3)(thiazole)]. Protein recognition and nucleotide excision repair of monofunctional adducts. Biochemistry. 42:792–800. PubMed

Loskotova, H., and V. Brabec. 1999. DNA interactions of cisplatin tethered to the DNA minor groove binder distamycin. Eur. J. Biochem. 266:392–402. PubMed

Nielsen, P. E. 1990. Chemical and photochemical probing of DNA complexes. J. Mol. Recognit. 3:1–24. PubMed

Zehnulova, J., J. Kasparkova, N. Farrell, and V. Brabec. 2001. Conformation, recognition by high mobility group domain proteins, and nucleotide excision repair of DNA intrastrand cross-links of novel antitumor trinuclear platinum complex BBR3464. J. Biol. Chem. 276:22191–22199. PubMed

Kartalou, M., and J. M. Essigmann. 2001. Recognition of cisplatin adducts by cellular proteins. Mutat. Res. 478:1–21. PubMed

Pil, P. M., and S. J. Lippard. 1992. Specific binding of chromosomal protein-HMG1 to DNA damaged by the anticancer drug cisplatin. Science. 256:234–237. PubMed

Wei, M., S. M. Cohen, A. P. Silverman, and S. J. Lippard. 2001. Effects of spectator ligands on the specific recognition of intrastrand platinum-DNA cross-links by high mobility group box and TATA-binding proteins. J. Biol. Chem. 276:38774–38780. PubMed

Kasparkova, J., O. Novakova, Y. Najajreh, D. Gibson, J.-M. Perez, and V. Brabec. 2003. Effects of a piperidine ligand on the mechanism of action of antitumor cisplatin. Chem. Res. Toxicol. 16:1424–1432. PubMed

Jung, Y. W., and S. J. Lippard. 2003. Nature of full-length HMGB1 binding to cisplatin-modified DNA. Biochemistry. 42:2664–2671. PubMed

Turner, R. M., N. D. F. Grindley, and C. M. Joyce. 2003. Interaction of DNA polymerase I (Klenow fragment) with the single-stranded template beyond the site of synthesis. Biochemistry. 42:2373–2385. PubMed

Villani, G., N. T. Le Gac, L. Wasungu, D. Burnouf, R. P. Fuchs, and P. E. Boehmer. 2002. Effect of manganese on in vitro replication of damaged DNA catalyzed by the herpes simplex virus type-1 DNA polymerase. Nucleic Acids Res. 30:3323–3332. PubMed PMC

Cohen, S. M., and S. J. Lippard. 2001. Cisplatin: from DNA damage to cancer chemotherapy. Prog. Nucleic Acid Res. Mol. Biol. 67:93–130. PubMed

Stehlikova, K., H. Kostrhunova, J. Kasparkova, and V. Brabec. 2002. DNA bending and unwinding due to the major 1,2-GG intrastrand cross-link formed by antitumor cis-diamminedichloroplatinum(II) are flanking-base independent. Nucleic Acids Res. 30:2894–2898. PubMed PMC

Delalande, O., J. Malina, V. Brabec, and J. Kozelka. 2005. Chiral differentiation of DNA adducts formed by enantiomeric analogues of antitumor cisplatin is sequence-dependent. Biophys. J. 88:4159–4169. PubMed PMC

Malina, J., J. Kasparkova, G. Natile, and V. Brabec. 2002. Recognition of major DNA adducts of enantiomeric cisplatin analogs by HMG box proteins and nucleotide excision repair of these adducts. Chem. Biol. 9:629–638. PubMed

Fuertes, M. A., J. Castilla, C. Alonso, and J. M. Perez. 2003. Cisplatin biochemical mechanism of action: from cytotoxicity to induction of cell death through interconnections between apoptotic and necrotic pathways. Curr. Med. Chem. 10:257–266. PubMed

Hoffmann, J.-S., M.-J. Pillaire, D. Garcia-Estefania, S. Lapalu, and G. Villani. 1996. In vitro bypass replication of the cisplatin-d(GpG) lesion by calf thymus DNA polymerase beta and human immunodeficiency virus type I reverse transcriptase is highly mutagenic. J. Biol. Chem. 271:15386–15392. PubMed

Suo, Z., S. Lippard, and K. Johnson. 1999. Single d(GpG)/cis-diammineplatinum(II) adduct-induced inhibition of DNA polymerization. Biochemistry. 38:715–726. PubMed

Novakova, O., J. Kasparkova, J. Malina, G. Natile, and V. Brabec. 2003. DNA-protein cross-linking by trans-[PtCl2(E-iminoether)2]. A concept for activation of the trans geometry in platinum antitumor complexes. Nucleic Acids Res. 31:6450–6460. PubMed PMC

Marini, V., P. Christofis, O. Novakova, J. Kasparkova, N. Farrell, and V. Brabec. 2005. Conformation, protein recognition and repair of DNA interstrand and intrastrand cross-links of antitumor trans- [PtCl2(NH3)(thiazole)]. Nucleic Acids Res. 33:5819–5828. PubMed PMC

Vaisman, A., S. E. Lim, S. M. Patrick, W. C. Copeland, D. C. Hinkle, J. J. Turchi, and S. G. Chaney. 1999. Effect of DNA polymerases and high mobility group protein 1 on the carrier ligand specificity for translesion synthesis past platinum-DNA adducts. Biochemistry. 38:11026–11039. PubMed

Gibbons, G. R., W. K. Kaufmann, and S. G. Chaney. 1991. Role of DNA replication in carrier-ligand-specific resistance to platinum compounds in L1210 cells. Carcinogenesis. 12:2253–2257. PubMed

Mamenta, E. L., E. E. Poma, W. K. Kaufmenn, D. A. Delmastro, H. L. Grady, and S. G. Chaney. 1994. Enhanced replicative bypass of platinum-DNA adducts in cisplatin-resistant human ovarian carcinoma cell lines. Cancer Res. 54:3500–3505. PubMed

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